Metatranscriptome data support the existence of two distinct morphotypes in a single parmalean species in natural environments

Abstract

Parmales (Bolidophyceae), the closest relatives of diatoms, includes isolates exhibiting one of two distinct morphotypes: a silicified non-flagellated form (S-type) and a naked flagellated form (F-type). Although alternation of these two forms for a single isolate has not been formally established, previous studies hypothesized that these morphotypes represent alternating stages of a single parmalean. In this study, we investigated the global expression patterns of S- and F-type marker genes by integrating parmalean Metagenome-Assembled Genomes (MAGs) and the metatranscriptomic dataset from Tara Oceans. We detected the expression of both S- and F-type marker genes from individual environmental MAGs. This finding provides the first metatranscriptomic evidence that natural parmalean genomes possess the potential to manifest both morphotypes. Furthermore, our analysis revealed different geographical expression patterns between the two forms. The expression of F-type markers showed a broad distribution, whereas that of S-type markers was more restricted, suggesting distinct niches for the two morpho-phases. Moreover, S-type gene expression appears to require specific environmental triggers that lead to a higher population density, whereas F-type expression is rather constitutively maintained. Overall, our results support the hypothesis of a life cycle involving morphological switching and reconcile the long-standing discrepancy between the ubiquity of parmaleans in molecular surveys and the limited geographical range for the observation of silicified cells. Based on these patterns, we propose a threshold-based model in which F-type-dominated populations persist under conditions unfavorable for growth and a morphological switch to the S-type is triggered once environmental conditions exceed a critical threshold for growth.